Interrelated chemical-microstructural-nanomechanical variations in the structural units of the cuttlebone of Sepia officinalis

L North,H B Caliskan,D Labonte,M L Oyen,R E Johnston,M P Coleman

doi:10.1063/1.4993202

Abstract

“Cuttlebone,” the internalized shell found in all members of the cephalopod family Sepiidae, is a sophisticated buoyancy device combining high porosity with considerable strength. Using a complementary suite of characterization tools, we identified significant structural, chemical, and mechanical variations across the different structural units of the cuttlebone: the dorsal shield consists of two stiff and hard layers with prismatic mineral organization which encapsulate a more ductile and compliant layer with a lamellar structure, enriched with organic matter. A similar organization is found in the chambers, which are separated by septa, and supported by meandering plates (“pillars”). Like the dorsal shield, septa contain two layers with lamellar and prismatic organization, respectively, which differ significantly in their mechanical properties: layers with prismatic organization are a factor of three stiffer and up to a factor of ten harder than those with lamellar organization. The combination of stiff and hard, and compliant and ductile components may serve to reduce the risk of catastrophic failure, and reflect the role of organic matter for the growth process of the cuttlebone. Mechanically “weaker” units may function as sacrificial structures, ensuring a stepwise failure of the individual chambers in cases of overloading, allowing the animals to retain near-neutral buoyancy even with partially damaged cuttlebones. Our findings have implications for our understanding of the structure-property-function relationship of cuttlebone, and may help to identify novel bioinspired design strategies for light-weight yet high-strength foams.

Highlights

Cuttlefish maintain near-neutral buoyancy at varying diving depths through the use of a specialized floatation device, frequently referred to as cuttlebone, which needs to combine high strength with minimum weight
The remarkable performance of the cuttlebone is linked to its structural architecture: cuttlebone is composed of calcium carbonate (CaCo3) in its aragonite polymorph with a mixture of β-chitin and other protein complexes, and comprises two main structural units: a dorsal shield and a series of chambers
The continuous chambers are separated by parallel septa and supported by a complex arrangement of meandering plates [from here on referred to as “pillars,” see

Summary

Introduction

Cuttlefish maintain near-neutral buoyancy at varying diving depths through the use of a specialized floatation device, frequently referred to as cuttlebone, which needs to combine high strength with minimum weight. 116103-3 North et al Mechanical properties of the different structural units of the cuttlebone were measured in ambient conditions with a TI 950 Triboindenter (Hysitron, Eden Prairie, USA), equipped with a diamond Berkovich indenter with a tip radius of 150 nm.

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